DOC removal paradigms in highly humic aquatic ecosystems

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Environ Sci Pollut Res (2009) 16:531–538 DOI 10.1007/s11356-009-0165-x

HUMIC SUBSTANCES • REVIEW SERIES

DOC removal paradigms in highly humic aquatic ecosystems Vinicius F. Farjalla & André M. Amado & Albert L. Suhett & Frederico Meirelles-Pereira

Received: 27 October 2008 / Accepted: 13 April 2009 / Published online: 22 May 2009 # Springer-Verlag 2009

Abstract Background, aim, and scope Dissolved humic substances (HS) usually comprise 50–80% of the dissolved organic carbon (DOC) in aquatic ecosystems. From a trophic and biogeochemical perspective, HS has been considered to be highly refractory and is supposed to accumulate in the water. The upsurge of the microbial loop paradigm and the studies on HS photo-degradation into labile DOC gave rise to the belief that microbial processing of DOC should sustain aquatic food webs in humic waters. However, this has not been extensively supported by the literature, since most HS and their photo-products are often oxidized by microbes through respiration in most nutrient-poor humic Responsible editor: Christian Steinberg V. F. Farjalla (*) : A. M. Amado : A. L. Suhett : F. Meirelles-Pereira Instituto de Biologia, Departamento de Ecologia, CCS, Ilha do Fundão, Universidade Federal do Rio de Janeiro, POBox 68020, CEP 21941-590 Rio de Janeiro, RJ, Brazil e-mail: [email protected] V. F. Farjalla Núcleo em Ecologia e Desenvolvimento Sócio-Ambiental de Macaé, P.O. Box 119331, CEP 28970-000 Macaé, RJ, Brazil A. L. Suhett Instituto de Biologia, Departamento de Ecologia, CCS, Ilha do Fundão, Programa de Pós-Graduação em Ecologia (PPGE/UFRJ), Universidade Federal do Rio de Janeiro, CEP 21941-590 Rio de Janeiro, RJ, Brazil Present Address: A. M. Amado Centro de Biociências, Departamento de Oceanografia e Limnologia, Universidade Federal do Rio Grande do Norte, Via Costeira, S/N, CEP 59014-100 Natal, RN, Brazil

waters. Here, we review basic concepts, classical studies, and recent data on bacterial and photo-degradation of DOC, comparing the rates of these processes in highly humic ecosystems and other aquatic ecosystems. Materials and methods We based our review on classical and recent findings from the fields of biogeochemistry and microbial ecology, highlighting some odd results from highly humic Brazilian tropical lagoons, which can reach up to 160 mg C L−1. Results and discussion Highly humic tropical lagoons showed proportionally lower bacterial production rates and higher bacterial respiration rates (i.e., lower bacterial growth efficiency) than other lakes. Zooplankton showed similar δ13C to microalgae but not to humic DOC in these highly humic lagoons. Thus, the data reviewed here do not support the microbial loop as an efficient matter transfer pathway in highly humic ecosystems, where it is supposed to play its major role. In addition, we found that some tropical humic ecosystems presented the highest potential DOC photo-chemical mineralization (PM) rates reported in the literature, exceeding up to threefold the rates reported for temperate humic ecosystems. We propose that these atypically high PM rates are the result of a joint effect of the seasonal dynamics of allochthonous humic DOC input to these ecosystems and the high sunlight incidence throughout the year. The sunlight action on DOC is positive to microbial consumption in these highly humic lagoons, but little support is given to the enhancement of bacterial growth efficiency, since the labile photo-chemical products are mostly respired by microbes in the nutrient-poor humic waters. Conclusions HS may be an important source of energy for aquatic bacteria in humic waters, but it is probably not as important as a substrate to bacterial growth and to aquatic food webs, since HS consumption is mostly channeled

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through microbial respiration. This especially seems to be the case of humic-rich, nutrient-poor ecosystems, where the microbial loop was supposed to play its major role. Highly humic ecosystems also present the highest PM rates reported in the literature. Finally, light and bacteria can cooperate in order to enhance total carbon degradation in highly humic aquatic ecosystems but with limited effects on aquatic food webs. Recommendations and perspectives More detailed studies using C- and N-stable isotope techniques and modeling approaches are needed to better understand the actual importance of HS to carbon cycling in highly humic waters. Keywords Bacterioplankton . Coastal lagoons . Dissolved humic substances . Dissolved organic carbon . Humic ecosystems . Microbial loop . Photochemical mineralization . Photo-degradation . Photo-oxidation

1 Background, aim, and scope Dissolved organic carbon (DOC) is a major carbon pool in the biosphere, and dissolved humic substances (HS) comprise 50–80% of DOC in aquatic ecosystems (Thurman 1985). Historically, HS were considered to be biologically inert in aquatic ecosystems, and their ecological functions were mostly related to iron and phosphorus bioavailability, pH control, and light penetration (Steinberg 2003; Steinberg et al. 2008). In 1974 and 1983, Pomeroy and Azam and co-authors introduced the microbial loop concept, in which DOC would enter planktonic food webs through incorporation into bacterial biomass and protozoan predation upon bacterial communities. Therefore, DOC and, more specifically, HS could be an important source of energy and matter to aquatic food webs. The carbon cycle in the biosphere and the CO2 flux between aquatic ecosystems and the atmosphere have recently received great attention due to the increase in the greenhouse effect. Planktonic bacteria, through aerobic respiration, may release a large amount of CO2 in aquatic

Environ Sci Pollut Res (2009) 16:531–538

ecosystems. In addition, the sunlight action on chromophoric humic carbon may produce CO2 in aquatic ecosystems, a process called photochemical mineralization. Bacterial and sunlight carbon mineralization, for instance, were responsible for 70% of total CO2 production in the water column of a temperate humic lake (Jonsson et al. 2001). Therefore, bacterial respiration and DOC photochemical mineralization play major roles in the net heterotrophy pattern found in most aquatic ecosystems. In the last few decades, several studies on bacterial DOC uptake and sunlight DOC photo-degradation have been performed in temperate ecosystems, resulting in several publications related to these processes (see del Giorgio and Cole 1998; Bertilsson and Tranvik 2000). Nutrient concentrations, temperature, and the quality of the DOC pool are major factors that limit bacterial DOC removal in aquatic ecosystems, and DOC concentration and quality and the amount of sunlight energy are major factors that regulate DOC photo-degradation. However, these processes were barely studied in highly humic ecosystems, where high rates of bacterial metabolism and DOC photo-oxidation are expected. Therefore, in these humic ecosystems, we expected a great importance of the microbial loop in carbon and energy fluxes throughout aquatic food webs. The tropical coastal lagoons of Rio de Janeiro State (Brazil) are shallow aquatic ecosystems formed by regression and transgression of the sea level during the Quaternary Period (Fig. 1a–c). These lagoons, which are separated from the nearby ocean by a sand bar, show a gradient of salt and carbon concentration related to their genesis. Humic coastal lagoons are orthogonally oriented in relation to the coastal line, show low salt concentrations, and are greatly influenced by the surrounding restinga mosaic vegetation (see Fig. 1a, b). The restinga vegetation exports large amounts of organic matter to these lagoons, which results in high DOC concentrations (10–160 mg C L−1), mainly composed of HS, and low water transparency. Bacterial and photodegradation of DOC in these tropical humic lagoons have been studied for many years, resulting in diverse publications (Granéli et al. 1998; Stepanauskas et al. 2000; Farjalla et al.

Fig. 1 Tropical coastal lagoons in southeast Rio de Janeiro State, Brazil. a Comprida Lagoon; b Cabiúnas Lagoon; c Garças Lagoon

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2002; Farjalla et al. 2006; Suhett et al. 2007; Amado et al. 2007) without being considered in a global context.

2 Materials and methods Here, we review basic concepts, classical studies and recent data on bacterial and photo-degradation of DOC, comparing the rates of these processes in highly humic ecosystems and other aquatic ecosystems. Furthermore, we also discuss the interaction between these two processes to total DOC degradation (i.e., complementarity or competition) and the actual trophic significance of the microbial loop in highly humic ecosystems. Finally, we have focused this review on results found in the highly humic tropical lagoons of Rio de Janeiro State (Brazil).

3 Results and discussion 3.1 Bacterial degradation HS stands for a group of complex organic carbon molecules in which each specific compound is present at very low concentrations (McKnight and Aiken 1998; Steinberg 2003). HS pools present high heterogeneity and are considered to be more refractory to bacterial growth than other carbon sources, such as the algal-derived DOC (Søndergaard and Middelboe 1995; del Giorgio and Davis 2003; Farjalla et al. 2006). An extracellular, enzymatic degradation step is required for bacterial uptake of humicderived carbon, and a cometabolism between more labile and abundant carbon molecules and HS has already been observed (De Haan 1974; Münster and De Haan 1998; Farjalla et al. 2009). However, because of their low degradation rates, HS may represent an important carbon source for bacterial metabolism in aquatic ecosystems (Tranvik 1998). Humic-rich aquatic ecosystems have a higher bacterial production potential than humic-poor ecosystems because of the higher carbon concentration in the former. The humic carbon content may shift a phytoplanktonic-based aquatic food web into a bacteriabased aquatic food web, with consequences to the balance between carbon emission and absorption in aquatic ecosystems (Jansson et al. 2000). Bacterial abundance and production would dominate the food webs and the energy flow in humic-rich aquatic ecosystems, where phytoplankton is usually limited by light penetration and inorganic nutrient competition with bacteria (Cotner and Biddanda 2002). Phytoplankton assemblages in these ecosystems are often dominated by mixotrophic flagellates that feed directly on bacterial cells (Jansson 1998). Therefore, the carbon flux through bacteria (i.e., the microbial loop)

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should be more relevant to aquatic food webs in humicrich ecosystems than in humic-poor ecosystems. However, the amount of humic carbon fixed by planktonic bacteria that reaches the higher trophic levels is still barely known (however, see Cole et al. 2006). Humic ecosystems are relatively carbon-rich and inorganic nutrient-poor ecosystems. Phosphorus is usually the main limiting nutrient for bacterial growth as well as DOC uptake in aquatic ecosystems (Vadstein 2000), and humic lakes are not an exception. For instance, bacterial growth in several humic lakes in northern Sweden that vary in total carbon concentration (2 to 20 mg C L−1) is phosphorus limited (Jansson et al. 1996; Jansson et al. 2000; Karlsson et al. 2001). We also observed a consistent phosphorus limitation in highly humic lagoons in southeast Brazil (10 to 75 mg C L−1, Farjalla et al. 2002). In addition, the quality of bulk DOC seems to play an important role by regulating the bacterial production in humic lagoons. After phosphorus addition, sequential addition of glucose significantly enhanced bacterial production despite the initially high DOC concentrations (Farjalla et al. 2002). Jansson et al. (2006) proposed that DOC is allocated to growth when bacteria are limited by low DOC concentrations as well as to respiration when bacteria are phosphorus limited. Therefore, we might expect higher rates of bacterial respiration in DOC-rich, phosphorus-poor aquatic humic ecosystems than in other aquatic ecosystems. In situ bacterial production varied from 0.014 to 1.418 μg C L−1 h−1 (N=19, median=0.139, 25–75 percentiles=0.084– 0.312, unpublished data and Farjalla et al. 2002) in Comprida lagoon, a highly humic coastal lagoon in Rio de Janeiro State (see Fig. 1a). In the same period, DOC concentration varied from 15.32 to 74.04 mg C L−1 (N=19, median=28.92, 25–75 percentiles=23.27–59.16, Farjalla et al. 2002; Suhett et al. 2007). Bacterial production in this lagoon is in the range found in the literature for aquatic ecosystems, but it is closer to the lowest limit of bacterial production values observed in lakes in a review performed by del Giorgio and Cole (1998). Bacterial respiration is less studied worldwide, but it seems to be less variable across ecosystems than bacterial production (del Giorgio and Cole 1998; Pace and Prairie 2005). In the same review, del Giorgio and Cole (1998) observed a positive correlation between bacterial production and respiration by using data from 237 paired analyses of bacteria production and respiration in the literature. Based on the two bacterial production × bacterial respiration alternative models that they proposed and on our values of in situ and in vitro measurements of bacterial production, we calculated significantly lower values of bacterial respiration than the ones we observed in three humic lagoons of Rio de Janeiro State (Fig. 2, see data in Farjalla et al. 2002). Therefore, bacteria in these highly humic lagoons showed proportionally lower

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Environ Sci Pollut Res (2009) 16:531–538

Fig. 2 Relationship between bacterial production and bacterial respiration in aquatic ecosystems. Models 1 and 2 are adapted from del Giorgio and Cole (1998). Bacterial production and respiration of tropical coastal lagoons (N=24) were based on Farjalla et al. (2002)

production rates and higher respiration rates than in other lakes (see Fig. 2), which resulted in low growth efficiencies (BGE, 10–14% during exponential growth, Farjalla et al. 2002). Such low BGE implies that only small amounts of humic DOC eventually reach higher trophic levels (Cole et al. 2006). Carbon and nitrogen isotopes have been widely employed to evaluate the consumer–resource interactions and carbon and energy fluxes throughout natural food webs (see review in Fry 2006). Primary producers differ in δ13C values due to differences in their CO2 fixation processes, and consumers keep the δ13C values close to that of their resources. Furthermore, there is a 3% enhancement of δ15N values between trophic levels in a food web; primary consumers, for instance, show δ15N values 3% greater than primary producers (Fry 2006). Therefore, the main carbon and energy sources of food webs may be revealed by carbon and nitrogen isotope techniques, despite some slight changes in δ13C values among trophic levels and confounding δ13C values among different primary carbon sources in complex natural ecosystems. In order to understand the roles of humic carbon and planktonic bacteria in the planktonic food web in highly humic lagoons, we have performed δ13C analysis of zooplankton and its potential carbon sources (phytoplankton, periphyton, DOC, particulate organic matter (POC), aquatic macrophytes, and terrestrial plants). Humic DOC and POC showed δ13C values similar to terrestrial plants and aquatic macrophytes, but zooplankton showed similar δ13C values to phytoplankton in these lagoons (Fig. 3). These results were very surprising since several studies have shown that bacterial growth based on humic DOC may contribute significantly to zooplankton growth (Karlsson et al. 2003, Daniel et al. 2005), and zooplankton may directly consume terrestrial POC, increasing its allochthony (Cole et al. 2006). However, some recent findings based on combined

Fig. 3 Carbon isotope analysis of planktonic organisms and carbon compartments in highly humic lagoons and surrounding terrestrial vegetation (unpublished data). Phytoplankton δ13C estimations were performed according to Mook et al. (1974) and Farquhar et al. (1982)

δ13C and carbon flux data have revealed that a large amount of bacterially metabolized humic DOC is lost through respiration compared to the amount transferred to zooplankton (
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